75

Invasive Insect and Nematode Pests
from North America
Keizi KIRITANI1 and Nobuo MORIMOTO2
1

1020-292 Futo, Itou City, Shizuoka 413-0231, Japan
E-mail: kiritanik@ybb.ne.jp
2
Department of Animal Breeding and Reproduction
National Institute of Livestock and Grassland Science
2 Ikenodai, Tsukuba, Ibaraki 305-0901, Japan
E-mail: morimoto@affrc.go.jp

Abstract
Of 447 alien insect, phytophagous mite, spider and nematode species in Japan, 415 are insect
species. Most were introduced after the end of the Edo period (1859). Coleoptera, Hemiptera,
Lepidoptera, Diptera and Hymenoptera represent the major taxonomic groups in decreasing order of
number of species. They include 58 insect and nematode species from the United States. Amongthem, the following three have been the most devastating North American species: the pine woodnematode, Bursaphelenchus xylophilus (the causal agent of pine wilt diseases transmitted by theJapanese pine sawyer, Monochamus alternatus), which was introduced in 1905; the fall webworm,
Hyphantria cunea (introduced in 1945); and the rice water weevil, Lissorhoptrus oryzophilus (1976).
Their range expansions and population dynamics after their establishment in Japan have been elucidated.
Explosive range expansions have always been associated with outbreaks of invasive insects. Changes
in future distribution ranges under global warming are discussed. Currently those introduced species
are becoming endemic as a result of various eco-physiological processes occurring after theirestablishment.
Key words: Bursaphelenchus xylophilus, exotic insects, fauna, Hyphantria cunea, Japan,
Lissorhoptrus oryzophilus, Monochamus alternatus, range expansion, USA

1. Introduction
Exotic pests are on the increase because of growth
in international air transport and tourism and increased
international trade in agricultural products, and also
because of growing human-dominated areas of disturbed habitat (Kiritani, 2001; Kiritani & Yamamura,2003).
Despite the deterrent effect of plant quarantine
regulations, accidentally introduced alien insect pests
continue to be added to the fauna of Japan (Morimoto& Kiritani, 1995; Kiritani, 1998, 1999). Kiritani andMorimoto (1993) and Morimoto and Kiritani (1995)
listed 324 species including 85 “possible” exotic
species of insects in Japan. Most of the species in
the latter group had been introduced to Japan before
the end of the Edo period (1859) when Japan started
conducting trade with Europe and the USA. Those“possible” alien species are called as “cryptogenic
species” (Carlton, 1996), meaning neither native nor
alien. Taking advantage of this unique politicalevent, we define “native” by reference to a cut-off
Global Environmental Research8(1)/2004: 75-88
printed in Japandate, i.e., 1859. Any species not already present inJapan that was introduced after that date is deemed
non-native. After that time, a large number of supplies were brought into Japan from abroad, accompanied by many kinds of alien insects.
Sometimes there is insufficient information available for analysis of exotic insect species. The
number of exotic species whose probable time ofinvasion is known is only 45% of the total and those
whose country of origin is known are only 40%(Kiritani & Yamamura, 2003).
Of a total of 447 alien insect, phytophagous mite,spider and nematode species (Kiritani, 2002), no lessthan 58 species originated from North America.
Among them, three species that have had a great
impact on Japan are the pine wood nematode(Bursaphelenchus xylophilus: Parasitaphelenchidae,
Nematoda), the fall webworm (Hyphantria cunea(Drury): Arctiidae, Lepidoptera), and the rice water
weevil (Lissorhoptrus oryzophilus Kuschel: Curculionidae, Coleoptera). These three species belong todifferent taxonomic groups and have unique life
©2004 AIRIES76

K. KIRITANI and N. MORIMOTO

histories.
Each of them has inflicted devastating damage toplants that characterize typical scenery in Japan,
namely, pine trees, cherry trees, and rice plants,
respectively. The magnitude of the damage they
have caused has been so great that it is possible toanalyze and compare their biological performancewith the help of information from various sources.
Case histories of these three highly damaging pests
may give us some ideas on vectors and pathways ofinvasive alien species and what happens in ecosystems
newly affected by biological invasions.

Table 1

2. Introduction of Alien Insects in Japan
from the USA
Despite the deterrent effect of plant quarantine
regulations, accidentally introduced alien insect pests
continue to be added to the fauna of Japan. Kiritani(2000) published a list of 45 insect species and anematode that have invaded Japan from the UnitedStates. Later, other species were added to the list.
The cumulative number from the United Statesamounted to 55 species as of 2003 (Table 1). The 55
species are comprised of 21 species of each of
Hemiptera and Coleoptera, 4 of Diptera, 3 of each of

Introduced species from the United States of America excluding natural enemies introduced for biologicalcontrol. Some species invaded Japan via other areas such as Pacific islands.
Insects: 57spp. Nematode: 1sp.

Order
INSECTA
Isoptera (3spp.)
Thysanoptera (2spp.)
Hemiptera (21spp.)

Coleoptera (21spp.)

Hymenoptera (2spp.)
Diptera (4spp.)

Lepidoptera (2spp.)
NEMATODA
Tylenchida (1sp.)

SpeciesYear foundSourceIncisitermes minor
Incisitermes immigrans
Zootermopsis nevadensis
Frankliniella occidentalis
Echinothrips americanus
Antonina graminis
Aphis oenotherae
Bemisia argentifolii
Corythucha ciliate
Eriosoma lanigerum
Genaparlatoria pseudaspidiotus
Hypogeococcus spinosus
Hysteroneura setariae
Icerya purchasi
Illinoia liriodendri
Kermes galliformis
Lepidosaphes ulmi
Melanaspis marlatti
Melanaspis obscura
Nearctaphis bakeri
Trialeurodes packardi
Trialeurodes vaporariorum
Uroleucon nigrotuberculatum
Uroleucon erigeronensis
Viteus vitifolii
Acanthoscelides obtectus
Adalia bipunctata
Araecerus fasciculatus
Brurchus rufimanus
Buprestis aurulenta
Callosobruchus maculatus
Diaachus auratus
Epilachna varivestis
Euscepes postfasciatus
Hypera postica
Hypera punctata
Lebia viridis
Lissorhoptrus oryzophilus
Listroderes costirostris
Olla v-nigrum
Ophraella communa
Psyllobora vigintimaculata
Sitona cylindricollis
Sitona flavescens
Sphenophorus venatus
Stenopelmus rufinasus
Sceliphron caementarium
Solenopsis geminata
Hermetia illucens
Liriomyza sativae
Liriomyza trifolii
Liriomyza huidobrensis
Hyphantria cunea
Parapediasia teterrella
Bursaphelenchus xylophilus

1975
1995
2000
1990
1999
1971
1990s
1989
2000
1872
?
1970s
1982
1908
1991
before 1986
1860s?
before 1986
1970
1974
1974
1991
1981
1882
1951
1993
1956
1926
1940
1950s
1995
1996 (1994?)
1947
1982
1978
1989
1976
1942
1987
1996
1984
1961
1986
1979
1987
1945
1967
1950
1999
1990
2003
1945
1964 & 1970
1905

Mori (1976)
Ohmura & Tokoro (2003)
Ohmura & Tokoro (2003)
Kiritani (2000)
Itoh & Ohno (2003)
Kiritani (2000)
Kagawa et al. (pers.com.)
Kiritani (2000)
Ishikawa (pers.com.)
Kiritani (2000)
Kiritani (2000)
Kiritani (2000)
Sugimoro (1995)
Kiritani (2000)
Sugimoto (1999)
Kiritani (2000)
Kiritani (2000)
Kiritani (2000)
Kiritani (2000)(Sugimoto pers.com.)
Kiritani (2000)
Kiritani (2000)
Otake (1999), Kiritani (2000)
Sugimoto (pers. com.)
Kiritani (2000)
Kiritani (2000)
Kiritani (2000)
Kiritani (2000)
Kiritani (2000)
Kiritani (2000)
Kiritani (2000)
Kiritani (2000)
Kiritani (2000)
Takara (1954)
Kiritani (2000)
Kiritani (2000)
Kiritani (2000)
Kiritani (2000)
Kiritani (2000)
Kiritani (2000)
Kiritani (2000)
Kiritani (2000)
Kiritani (2000)
Kiritani (2000)
Kiritani (2000)
Kiritani (2000)
Kiritani (2000)
Kiritani (2000)
Kiritani (2000)
Kiritani (2000)
Kiritani (2000)
Kiritani (2000)
Kiritani (2000)
Kiritani (2000)

Invasive Insect and Nematode Pests from North America

Table 2The number of species which invaded Japan fromthe US.

PeriodNo. species

1859–1939

6*

1940–196911

1970–1999
33 ***: including the pine wood nematode.
**: three species invaded after 2000.

Early summer

July–next June

Pine forests in Japan occupy about 2.5 million ha,accounting for about 10% of forested land. Pine
trees have been economically important from ancient
times, mainly as fuel for domestic and industrial uses
and as lumber for building. The decline of pine
forests in Japan has seriously affected soil and water
conservation and, consequently, agriculture and aquaculture. Loss of ornamental pines to pine wilt
disease has had an impact on Japanese culture as well
(Kobayashi et al., 1984; Kobayashi, 1988).
Epidemics of pine wilt disease caused by the pine
wood nematode (PWN), Bursaphelenchus xylophilus,
whose vector is the Japanese pine sawyer (JPS),
Monochamus alternatus, are killing pine forests
throughout Japan. The major pine species, Japanese
red pine (Pinus densiflora) and Japanese black pine (P.
thunbergii) have suffered heavy mortality for several
decades. The foliage of infected trees quickly fades
to a reddish-brown. Most trees naturally infectedwith nematodes die within a year of infection, usuallyby late autumn, in warm temperate climatic zones(Fig. 1).
Ecological and biological characteristics of the two

3. Pine Wilt Disease

key species are as described below.
PWN (Bursaphelenchus xylophilus): Widespread
distribution of this nematode was reported in the
United States (Wingfield et al., 1982), where only
exotic pine plantings are severely damaged, suggesting that the nematode could have been accidentally
introduced into Japan from the United States. Thisview has been supported by DNA sequence comparison between isolates of B. xylophilus from bothcountries (Harmey & Harmey, 1993; Tarès et al.,1993). Nagasaki, where the first pine wilt disease
outbreak was recognized in 1905, was the mostprosperous international trading port at that time.
JPS (Monochamus alternatus): The JPS has beenrecorded in mainland China, Taiwan, Laos, Korea(Cheju Is.), and Japan (Table 6). It normally produces one generation a year and is widely distributedin Japan, except for Hokkaido and northern Honshu.
Its distribution in both Okinawa Prefecture and the
Ogasawara Islands is considered to be due to recent
introductions of infested pine logs. The factor
limiting its distribution in northern Honshu is the lackof sufficiently high temperatures in summer, not the
low temperatures in winter (Makihara, 1997).
3.1 Epidemics of pine wilt disease
The decisive factor in developing epidemic infestation in Japan was the contact between sawyers andnematodes. The JPS is native to Japan but was arather scarce insect until it came into contact with the
PWN. The spread of disease is facilitated by an obligatory mutualism between PWN and JPS: the JPS
helps the PWN be transmitted to a new host tree,
while the PWN supplies the JPS with newly killedtrees on which to lay eggs (Fig. 1).
The JPS adults emerge in early summer and feedon young twigs for maturation, meanwhile PWN
dauerlarvae invade healthy pine trees. Once within

June–Aug.

Isoptera, and 2 of each Lepidoptera, Hymenoptera andThysanoptera. They are arranged by their year of
detection in chronological order with an interval of 10
years, except for four species whose times of
introduction are not known (Table 2). The total
number of species becoming established per 10 years
in Japan has also increased during the past 140 years.
It is possible to divide the 140 years into the following
three phases in terms of the frequency of invasions,
1860–1939, 1940–1969 and 1970–1999. The frequency of invasion during 1970–1999 was as high as
10 times that in 1860–1939, and it is expected that one
new species will become established in Japan everyyear.
In the following accounts, we elucidate the invasive histories of three exotic species originating fromthe USA. Each of them demonstrates unique characteristics in terms of range expansion, population
dynamics, and evolutionary perspective. They also
represent pests of forests, urban areas, and agricultural
crops, and invaded Japan in 1907, 1945 and 1976,
each representing three different phases of invasions
in Table 2.

77

No. species/year
0.1
0.4
1.1










Fig. 1 Epidemic cycle of JPS-PWN-Pine tree.

78

K. KIRITANI and N. MORIMOTO

the plant, the nematodes reproduce rapidly and theinfected tree shows symptoms of decline about three
weeks later (Kobayashi et al., 1984). The weakened
pine trees provide JPS females with oviposition sites.
Dead trees are not available for oviposition and will
never serve as infection sources again. Once thenematode is introduced into the sawyer – pine treesystem, the beetle increases its own food supply bytransmitting nematode during maturation feeding,resulting in an unstable interaction system (Fig. 1).
Consequently during a four-year study the net
reproduction rate (Ro) of the JPS varied greatly from
5- to 11-fold (Togashi, 1989). A 10-year-old plantation of Pinus thunbergii located in central Honshu
exemplifies the epidemic (Table 3) (Kobayashi, 1978).
The annual mortality of pine trees was about 5% in astand free from the PWN, while stands infected by the
PWN resulted in mortalities of 25% in Hirosima, and17%, 37% and 44% in Ibaraki, giving 30% as a meanmortality (Togashi, 2002).
3.2 Range expansion
After a latent period of two decades, the infestation
spread rapidly through Kyushu into western Honshu.
During the war, annual tree losses increased, reaching
1.3 million m3 in 1948. Outbreaks were encouragedby the collection of turpentine oil from pine trees
which provided weakened trees for oviposition.
Control operations helped by the utilization of killedtrees as fuel resulted in decreased infestation in the
1950s. At the beginning of the 1970s, however, therate of infestation started to rise again because of thechange to petroleum as Japan’s major energy source
and a lack of labor for control operations. In 1978
and 1979, largely because of hot, dry summers thatencouraged epidemics, annual tree losses amounted to
2 million m3/year (Fig. 2). In 1979, 650,000 ha, 25%of the total pine forest area, was affected by thedisease, and the annual loss of timber reached arecord-breaking 2.4 million m3. A nationwide control
project was started in 1977 and about $30 million is
now spent annually on spraying and treating infested
logs. Annual tree losses have gradually decreased,
but infestations have spread into northern Honshu andinto forests at higher elevations (Fig. 2 & Fig. 9, left).
In general, both temperature and precipitation areimportant factors that affect the severity of damage by

PWN. High temperature and low precipitation insummer cause accelerated damage. Because of theireffects on feeding by JPS adults, the propagation of
PWN and water stress on trees. Pine trees infectedwith PWN show cessation of oleoresin exudation, asymptom of disease, over the period from June to
October (Mamiya, 1983). Females that emerge fromdead trees in June and July lay eggs on weakened
trees until September. Therefore, the extent to which
their oviposition and the appearance of weakened
trees overlap is decisive in determining the severity ofthe epidemics. Delayed appearance of weakened
trees in a cool and rainy summer climate, therefore,
results in a less intense epidemic (Togashi, 1989).
An MB index that combines temperature conducive to JPS development, PWN infection and tree
weakening has been proposed as a measure ofinfestation potential (Taketani et al., 1975). This is
the annual summation of residues of mean monthly
temperature exceeding 15°C. Epidemic pine infestations nearly always correspond to areas with an MB
index exceeding 40. Such areas are located mainly
along the coast and inland along river valleys up to
about 200 m above sea level. In general, damage
due to the PWN hardly ever occurs in areas where themonthly mean temperature from June to August is
below 20°C.
3.3 Pathogenic variability
When tested on 4-year-old Japanese black pines inJapan, the virulence of 37 populations of PWN varied
from 0 to 100% in terms of pine tree mortality. Fourof the most virulent populations were recovered from
northern Japan where establishment was relatively
recent (Kiyohara & Bolla, 1990). In the USA where
the PWN is native and widely distributed, the occurrence of pine wilt disease is rarely observed, except in
the case of some exotic pine plantings. It is known
that Pinus strobus and P. taeda are resistant to the
PWN infection (Kiyohara, 1997).
The myxoma virus, introduced into Australia tocontrol rabbits, underwent a rapid attenuation ofvirulence, measured in terms of lethality to a standard
susceptible population (Fenner & Ratcliffe, 1965). It
is our concern whether and when the current unstablesystem of pine wilt disease will become stabilized.
That less virulent races have been found more

Table 3 Annual change of pine tree mortality in a severely infested forest located at Hikigawa, Wakayama(Kobayashi, 1978).
1967

1968

1969

1970

1971

1972

1973

1974

*

*

*

*

0

No. of trees living at the
beginning of the year

455

435

379

237

52

23

4

No. of trees killed

20

54

141

179

15

19

4

% trees killed

4

12

37

73

29

83

100

* No. of trees is not equivalent to the remainder subtracted from the number in the previous year because of
felling of living trees alive.

Invasive Insect and Nematode Pests from North America

Fig. 2

79

Annual changes in pine tree loss due to pine wilt disease (-{-) and in the
cumulative number of prefectures infected by the PWN (-U-) (revised by Kishi,
1988).

frequently in southwestern Japan where epidemics
occurred earlier, and that pine trees which survive an
epidemic are more resistant to the disease (Toda,
1997) suggest the possible existence of moderate
virulence once the feedback between ecological andevolutionary processes is incorporated into the system(Lenski & May, 1994; Togashi, personal communication). It is still too early to predict when the current epidemics will shift to an endemic state, because
only 100 years (a few generations of pine stands) havepassed since the PWN invaded Japan.

4. The Fall Webworm (FWW), Hyphantria
cunea
4.1 Invasion and range expansion
In North America, the fall webworm (FWW),
Hyphantria cunea, is found over a wide area extending from Canada to Louisiana. The FWW occurred
only in North America before 1940, but was
subsequently introduced to central Europe and eastern
Asia during the 1940s by human activities (Warren &Tadic, 1970). Two color forms of the FWW are
known in North America. The type introduced into
Japan, as well as into Korea and Europe, belongs tothe black-headed form and is quite distinct from the
red-headed form reported from Louisiana (Oliver,
1964; Itô & Hattori, 1973).
The FWW was first found in Tokyo (35.7oN) in
1945, two months after the end of World War II (Table6), and since then has caused great damage to garden
and roadside trees. It has spread along highways andrailways in association with its outbreaks (Masaki,1975). The first outbreak lasted from 1945 to 1957,
and the second, from 1964 to 1968 after an endemic
stage from 1958 to 1964 (Itô & Miyashita, 1968) (Fig.
3). The number of prefectures infested by the FWW
in the second outbreak reached 21 (Fig. 3). Thereafter, the rate of expansion decreased, with sporadic

occurrences in neighboring prefectures. The present
distribution ranges from 32oN to 41oN, covering atleast 35 of the 47 prefectures in Japan (Gomi, 1999)(Fig. 9, middle).
4.2 Population dynamics and natural enemies
An outstanding feature of FWW infestations is thatthe occurrence of FWW is rarely observed in forests,
but is confined to trees along roadsides and inresidential areas. The failure of FWW to invade
forests is due to predation pressure by birds and otherpolyphagous predators. The factor responsible forkeeping the population density low during 1958–1964
was those natural enemies of FWW (Itô & Miyashita,1968). Life table studies conducted by Itô andMiyashita (1968) showed that mortality from egg to
the 4th instar was 20% to 70%, while that from the 5th
instar to pupa was over 96% during 1966–1969 at two
experimental stations (Table 4). The low mortality
rate in early stages is considered due to the protectiverole of the nest-web and being free from egg andlarval parasitoids. Watanabe (personal communication), who conducted an intensive survey on theparasitic fauna of FWW larvae during 1995–1997 in
Tsukuba, found no hymenopterous parasitoids but 6
species of tachinids that are generalists in host
preference. The highest rate of parasitism due to thetachinid complex was 70%–80% in 3rd-generation
larvae in the wandering stage.
Mortality during later stages is mainly due topredation by birds in the first generation and Polistes
wasps in the second generation (Itô & Miyashita,1968). It is interesting to compare the number of
spiders inhabiting FWW webs between Japan andNorth America (Table 5). Two hundred fifty-fivespiders, representing 34 species and 10 families, wererecorded from 248 FWW webs in Tokyo (Kunimi,1983). The mean number of spiders per web was as
small as 0.37, compared to 1.26 in Arkansas (Warren
et al., 1967), 2.28 in New Brunswick, and 3.01 on the

80

K. KIRITANI and N. MORIMOTO

coast of Nova Scotia in Canada (Morris, 1972) in the
countries of origin of FWW.
The extent at which Liquidambar styraciflua L.
trees along the roadside in Tsukuba were defoliated by
the FWW correlated positively with the index ofurbanization, which is expressed in terms of the proportion of plant ground cover (Fukuyama, 1996).
Fukuyama (1996) considered the paucity of polyphagous natural enemies caused by urbanization as afactor in severe defoliation by the FWW.
4.3 Development of a trivoltine race
The bivoltine life cycle of the FWW in Tokyo isclearly explained by the photo-thermal reaction. In

Fig. 3the larval stage of the summer generation, the day
length exceeds the critical level (14 hr. 35 min. at
17–27°C) and diapause is averted. It becomesshorter than the critical level for the next brood, andthe pupae enter diapause and hibernate (Masaki, 1975).
It is predicted that the FWW will be unable to invade
Hokkaido where the available heat units could permit
only one generation a year. The long days in summer,
however, would prevent diapause. In the southernpart of Kyushu and Okinawa, the warm climate would
allow at least three or four broods a year, but the day
length becomes shorter than the critical level long
before winter. This would make it difficult for the

Annual changes in number of trees infested by FWW (-{-) and infested prefectures (-U-)
in Japan.

Table 4 Mortality rates of the fall webworm in the periods from egg to 4th instar and from 5th instar to pupa
observed at two experimental sites in Tokyo during 1966 – 1969. (Itô & Kiritani, 1971)
Year

Generation

1966

1st generation
2nd generation
1st generation
2nd generation
1st generation
2nd generation
1st generation
2nd generation
1st generation
2nd generation

1967
1968
1969
Mean

Nishigahara, Tokyo
Egg-L4L5-Pupa
60%
98.4%
69
98.8
67
99.2
61
99.6
61
96.4
51
99.5
52
99.3
20
99.6
60
98.3
50
99.4

Futyu City, Tokyo
Egg-L4L5-Pupa
65%
99.1%
71
99.9
36
99.8
50
99.0
29
97.8
38
98.2
69
95.5
58
97.7
53
98.1
54
98.7

Table 5 Mean numbers of spiders collected from nests of the FWW in different countries.
Country
USA
CanadaCanadaJapan

Arkansas
New Brunswick
Nova Scotia
Futyu City, Tokyo

No. spiders / nest
1.26
2.28
3.01
0.37

Authors
Warren et al., 1967
Morris, 1972
Morris, 1972
Kunimi, 1983

Invasive Insect and Nematode Pests from North America

FWW to become established in Okinawa (Masaki,1975). Masaki (1975) suggested that the seasonal
life cycle may change in the future through natural
selection.
Among insects inhabiting temperate areas, there isa general tendency for northern populations to enter
diapause earlier in the year under longer day lengths
than the southern ones (Masaki, 1975). In the
mid-1970s, three decades after the introduction of the
FWW to Tokyo, a partially trivoltine life cycle wasreported in the southwestern part of Japan (Uezumi,1976). Recently, trivoltine populations have prevailed in the southwestern areas and bivoltine ones in
the northern areas (Gomi, 1999; Gomi & Takeda,
1996).
The critical photoperiod was longer in bivoltine
populations north of 36oN than in trivoltine populations south of 36oN. The durations of the larval andpupal stages were shorter in the southern populations
than in the northern ones. Thus, both the criticalphotoperiod and developmental rate changed when theshift in voltinism from bivoltine to trivoltine occurredas this insect expanded its range (Gomi, 1999). It
has been confirmed by the DNA sequence of thecytochrome c oxidase subunit I gene that, in spite ofthe divergent life cycles of FWW in Japan, the variation in voltinism has been established by natural
selection after introduction and is not due to multiple
introductions from different parts of the USA (Ozaki& Ohbayashi, 2001). Masaki (1977) predicted that
the FWW would establish a clear geographic cline in
the critical photoperiod in the future. It would beinteresting to find out how long it will take the FWW
to form such a cline in Japan.

5. The Rice Water Weevil (RWW),
Lissorhoptrus oryzophilus Kuschel
5.1 Invasion and range expansion
The RWW is the most common and probably themost destructive insect pest of rice in the UnitedStates. The insect in the southeastern part of the
USA reproduces bisexually. The presence of RWW
in the rice-growing area of California, where it reproduces parthenogenetically, was first reported by Lange
Table 681

in 1959 (Bowling, 1967).
The RWW, which is likely to have invaded Japan
from California, was first found on the Chita peninsula, Aichi Prefecture, in 1976 (Table 6). At thattime, stock farmers on the Chita peninsula imported
hay from California. The Japanese RWW reproduced parthenogenetically as in California (Tsuzuki etal., 1984). It had become distributed throughout
Japan by 1986. Subsequently, the RWW invaded
Korea in 1988 (Lee & Chang, 1989), mainland China
in 1988 (Hirai, 1996), and Taiwan in 1990 (Shih,1991). The maximum area of rice fields infested by
the RWW in Japan was observed around 1990 andamounted to 1,440,000 ha (Fig. 4).
The RWW overwinters in adult diapause which
terminates by December (Morimoto, unpublisheddata). The overwintered adults develop flight muscles by feeding on the leaves of Gramineae andCyperraceae plants (Okada, 1980). They invade
paddy fields by crawling or flying when rice plants aretransplanted. Ovarian development takes place as aresult of feeding on rice plants. The larvae feed on
the roots of rice plants and pupate there. Newly
emerged adults disperse to overwintering sites(Asayama et al., 1984).
The range expansion of the RWW in each prefecture of Japan has been described in detail (Azuma etal., 1991). The spatial expansion rate of the RWW
within a prefecture was calculated using a logistic
equation;Y = m1 / {1 + exp [− m2 × (T − m3)]}
where Y is the area of rice fields (ha) infested by the
RWW, T is the year, and m1, m2 and m3 are constants.
The three parameters (m1, m2 and m3) were estimatedusing the least-square method. The tangent line at
the point of inflection of each curve was computed as
R = m1 × m2 / 4
where R is the slope of the line. The slope is definedas the expansion rate of the RWW in each prefecture.
The expansion rate was significantly negatively
correlated with latitude (R = 0.76) among the prefectures located between 30oN and 40oN (Fig. 5).
Andow et al. (1993) reported that the distribution
boundary line varied with time and was dependent on
direction. The progression rate of the boundary line

Range expansions of the pine wood nematode (PWN), fall webworm (FWW) and rice water weevil (RWW),
in Japan and to neighboring countries.

MainlandOkinawa
Ogasawara
Korea
TaiwanChina

PWN
1905 (Nagasaki),absent from Hokkaido
1973 1)1974 3)1988 (symptoms
observed since 1983) 5) 3)
1985 5)
1982 5) 9)

FWW1945 (Tokyo),and in 2000 in Hokkaido 10)
absent1994 (trivoltine type) 4)
1958 in Soul 6)

RWW
1976 (Aichi) andin 1986 in Hokkaido
1985 2)---1988 7)

absentoccurs commonly 6)

1990 8)1988 2)

1) Kishi (1988) 2) Hirai (1996) 3) Makihara (1997) 4) Ohobayashi (2002) 5) Kiyohara (1997)
6) Gomi(1996) 7) Lee and Chang (1989) 8) Shih (1991) 9) Sun (1982) 10) Tate (2001)

82

K. KIRITANI and N. MORIMOTO

was initially between 28 km/year northeastwardly and
47 km/year southwestwardly; it increased to about
274 km/year and 113 km/year, respectively, 7 years
after the initial invasion.
The most important factors in the range expansionof invasive organisms are reproduction rate anddispersal ability (Hengeveld, 1989; Andow et al.,
1993; Williamson, 1996; Shigesada, 1992). The
active adult dispersal of the RWW between hibernacula and paddy fields can be observed only inspring and late summer, because the degeneration of
the flight muscle prevents RWW adults from dispersal
by wing at other times (Matsui, 1985). It has been
pointed out that wind plays an important role in thelong-distance dispersal of the RWW (Kishimoto,1980; Muramatsu & Tao, 1981; Tsuzuki et al., 1984).
In general, low-pressure air masses, typhoons, andprevailing westerlies move from west to east over theJapanese Islands. Accordingly, the founding RWW
population established in central Japan may disperse
eastwards with the movement of these air masses(Kobayashi & Suzuki, 1983; Kaneko et al., 1984).
Because it takes some time for any newly invading
population to reach a detectable level of density, it isdifficult to identify a causal relationship between aparticular weather condition and the range expansionof the RWW.
There is a great difference in the intensity of RWW
occurrence between north and south. The percentages of paddy fields infested by the RWW were 57%
and 27% in Tohoku (north) and Kyushu (south),respectively, in 1995 (MAFF, 1996). Transplantingof rice occurs earlier in areas further north (Fig. 6).
The RWW density is higher in localities where rice istransplanted early than elsewhere (Izawa et al., 1984;
Naba et al., 1989; Kobayashi et al., 1997). In
southern Japan, invasions of the RWW used to be
detected first in each prefecture in the localities where
rice was transplanted earliest (Higo et al., 1986; Nagai

Fig. 4& Teramoto, 1985; Ogawa et al., 1989; Yamanaka etal., 1985). These findings strongly suggest that the
population dynamics of the RWW are closely related
to the time of transplanting of rice.
Adults that have overwintered in northern areas
can access rice plants much earlier than those insouthern areas, and it is highly probable that they canrealize their potential fecundity as well as enjoy a highsurvival rate (Figs. 7A & 7B). The flight muscles of
the RWW are not fully developed by the time of transplanting of rice in northern areas, and most of theadults immigrate into the rice fields by walking (Figs.
7A, 7B & 7C). By contrast, overwintered adults areable to access to rice plants by flight in southern Japan(Figs. 7C, 7D), but their fecundity is greatly diminished due to the low survival rate and aging during thelong waiting period for transplanted rice (Figs. 7D &7E). As this process is repeated year after year, theRWW population density in northern areas becomeslarger and eventually the rate of spread accelerates.
5.2 Population dynamics
Over the last decade, the RWW’s rate of spread has
decline and it now occurs in half of the total area ofrice fields of Japan (Fig. 4). Changes in the mean
total number of larvae and cocoons found per hill are
shown in Fig. 4 in non-treated plots of experimental
rice fields located in 11 prefectures in the Kanto andTokai areas. The density was initially around 20
individuals per hill, and it increased up to 30 in 1985
when the RWW had spread throughout Japan (except
for Hokkaido) (Figs. 4 & 9). Thereafter, it declined
in a saw-tooth pattern to less than 10 in 1995 (Hirai,
2000). Recently it has again shown an increasing
trend in density, but the reason remains to be known(Fig. 4). Almost the same results were obtained in
Nagano prefecture in terms of the population densityof overwintered adults from 1985 to 1994 (Kobayashi
et al., 1997).
The population density seemed to stabilize 4–5

Annual changes in area infested by RWW(-{-), number of prefectures infested(-U-), and the density of immature RWW per hill (-■-).

Fig. 5 Expansion rates of RWW in 44 prefectures in relation totheir latitudes. The southernmost (Okinawa) andnorthernmost (Hokkaido and Aomori) prefectures were
excluded.
Each circle represents an individual
prefecture.

83

Performance of Rice Water Weevil

Invasive Insect and Nematode Pests from North America

Day - degrees
Fig. 6 Date of transplanting of rice in the 44 prefectures inrelation to their latitudes.

years (generations) after invasion. The RWW population density appeared to be regulated mainly bydensity-dependent processes that operated between
oviposition and the emergence of young larvae.
Fecundity decreased with increasing density of over
two adults per hill. Population density was dependent on the mortality rate from egg to young larva,
and this was the key factor determining the generationmortality from egg to the emergence of the adult(Kayumi et al., 1984).
The pattern of population growth can be simulated
by a logistic equation:(Nt+1 + Nt) / Nt = R (1 + Nt / K)
where Nt and Nt+1 are the numbers of overwinteredadults per hill in years t and t+1, R is the rate ofannual increase, and K is equilibrium density. K
seems to be determined by the availability of overwintering sites and the date of transplanting or availability of rice plants for overwintered adults. K was
estimated at 0.38, 1.78, and 2.44 adults/hill for coastal
areas, inland hilly areas, and mountainous areas,
respectively (Fig. 8) (Kayumi et al., 1984).
So far, no evidence has been obtained concerning
the effect of natural enemies of the RWW. This ispartly due to the submerged life cycle of the RWW,
which prevents us from making direct observations ofFig. 7

Fig. 8Difference between southern and northern
Japan in the extent to which the potential
fecundity of the RWW is realized. Egg
maturation occurs after feeding on rice
plants.

Reproduction curves and equilibrium densities
in the areas with different topography. (after
Kayumi et al., 1984).

84

K. KIRITANI and N. MORIMOTO

the activities of predators. The recent reduction in
the RWW population density and the size of areas
infested may be largely attributable to the widespread
application of pesticides to the nursery trays before
the rice is transplanted.

6. Discussion
The biological process of colonization by alienorganisms can be categorized in the following four
steps: introduction, establishment, spread, and naturalization (Kiritani,1998). Several attempts have been
made to characterize successful and unsuccessful
invaders (Kiritani, 1983; Ehrlich, 1988; van Lenteren,
1995; etc.). Characteristics of successful invaders
such as polyphagy, multivoltinism, parthenogenesis,
anthropogenic inhabitant, and good dispersal capability are generally accepted by most ecologists.
However, there are so many exceptions that it is notjustifiable to use these characteristics as reliable indicators of a species' potential to invade (Ehrlich, 1988;
van Lenteren, 1995). Indeed, the RWW, a typicalexample of an invasive pest of agricultural crops, isunivoltine and monophagous.
The range expansions of the PWN, FWW, and
RWW in Japan and their hypothetical reproduction
curves are summarized in Fig. 9. The FWW spreadfrom Tokyo to other parts of Japan assisted by transportation systems or by hitchhiking. Its range expansion was limited by its genetic variability in terms ofthermo-photoperiodism, which determines its life
cycle in a newly invaded area.
The RWW showed a continuous diffusion with the
spread rate accelerating with time. The speeds at
which the RWW spread its range were 28 km/year to

Fig. 9the north and 47 km/year to the south in the earlyphase of range expansion (Andow et al., 1993). The
range of the RWW depends on the availability of rice
plants. Therefore, it is distributed throughout Japan,
including the Nansei islands (Okinawa).
The pattern of range extension of the PWN/JPS isa mixture of hitchhiking and continuous diffusion
types. Hengeveld (1989) called this type of range
expansion stratified diffusion, as it involves not only
short-distance dispersal, but also long-distance dispersal. Takasu et al., (2000) estimated the speed ofrange expansion as 4.2 km/year for short-distancedispersal. The PWN/JPS was prevented from spreading further by the cool, wet summers prevailing in theinvaded area.
The patterns of population dynamics of the above
three species were also species specific. The FWW
suffered mortality due to generalist natural enemies.
It showed gradation-type outbreaks when it escapedfrom the control exerted by natural enemies. On theother hand, there were no observations of arthropod
natural enemies of the RWW. Density-dependent
processes involving changes in fecundity and survival
rate in earlier developmental stages were suggested as
regulatory factors. The density tended to stabilize
after 4–5 years of invasion, fluctuating around an
equilibrium density specific to each locality.
The PWN/JPS system is unique. The JPS is
attacked by microbes, nematodes, arthropod predators,
and parasitoids. It is regulated by density-dependentmortality in the early larval stages (Kobayashi, 1988;
Kobayashi et al., 1984). When the JPS comes into
contact with introduced PWN, pine wilt disease
epidemics become destructive and continue until
entire pine stands are destroyed.

Range expansions and reproductive curves of the pine wood nematode (PWN), the fall webworm(FWW), and the rice water weevil (RWW) in Japan. For range expansions, see also Table 6.

Invasive Insect and Nematode Pests from North America

Our analyses demonstrated that ecological andphysical conditions in the invaded areas were of paramount importance in determining the status of colonizers after establishment. In particular, climaticconditions, natural enemies, distribution patterns ofhost plants, genetic variability, and synchronization oflife cycles of insects and their hosts were the factorsthat determined population density and the expansion
rate of colonizers. Concerning the long-distance expansion of successful invaders, it should be emphasized that explosive range expansions involving
neighboring countries, i.e., Taiwan, Korea, and mainland China, were always associated with outbreaks of
the invasive insects in Japan.
The Intergovernmental Panel on Climate Change(IPCC) (2001) has predicted that the global-meansurface temperature will increase 1.4–5.8°C by theyear 2100 as compared to 1990. Such an increase intemperature may result in an increase in number ofgenerations per year and in a shift of the distribution
range of most insects (Morimoto et al., 1998;
Yamamura & Kiritani, 1998). The reproductive performance of the RWW depends greatly on temperature,and the RWW lays the highest number of eggs withthe shortest preoviposition period at 32°C within atemperature range of 15–32°C (Morimoto, unpublished data). In order to fully realize RWW fecundity,
the existence of rice plants is essential. If the time ofrice transplanting should advance accordingly, theoverall population density of the RWW would be
expected to increase under global warming. As thecurrent distribution of pine wilt disease is limited by
low temperatures in summer, not only would pine wilt
disease extend its distribution to Hokkaido, but also
the intensity of epidemics would increase in thenorthern part of Japan (Table 6). In the case of the
FWW, the trivoltine race would become predominanteven north of 36oN. Range expansion further northor south beyond the current distribution would depend
on whether the FWW could adjust its temperature aswell as photoperiod responses to new environmental
conditions in the foreseeable future.
Current control measures
The distribution ranges of the PWN, FWW and
RWW cover almost all of Japan. Because it is impossible to eradicate them, we must adopt an IPM
strategy to control them. In this section, current control measures were reviewed.
PWN: The JPS which serves as the vector for the
PWN has been controlled with insecticides. Aerial
spraying of insecticides by helicopter was commonly
practiced in some parts of Japan. This widespreadchemical control may seriously affect the biodiversityof pine forests. Trunk injection of nematocides(nematicides) is one of the alternatives, but this mustbe performed before any symptoms occur and is laborconsuming. Research is now being conducted on thepossibility of breeding resistant pines, as different

85

degrees of resistance can be observed among various
strains of pine trees.
FWW: Mainly insecticides have been used against
the FWW since its occurrence.
Konno (1998)
reported that FWW larvae had developed resistance tosome insecticides
RWW: Farmers usually apply insecticide tonursery boxes before transplanting. The area treatedcovered 665,568 ha in 2000 which represented onethird of the paddy fields in Japan. No efficientnatural enemies have been detected in either the USA
or Japan. Two kinds of filamentous bacteria, whichwere introduced into rice fields, showed no appreciable effect on the RWW population (Hirai, 2000).
Draining surface water for 2 weeks from paddy fields
decreased the densities of the RWW (Shimohata &Kanoh, 1983). About 150 rice varieties originatingin Japan or other countries were screened for tolerance
to injury by this insect. A few varieties showedtolerance (Shaku et al., 1984). However, thosecultural control methods are mostly in an experimental
phase.

Acknowledgements
We thank, K. Fujita, T. Gomi, F. Kobayashi, K.
Kunimi, K. Togashi, Y. Watanabe and K. Yamane for
their comments and permission to use unpublisheddata and D. Andow for a critical reading of themanuscript.
References
Andow, D.A., P.M. Kareiva, S.A. Levin and O. Okubo (1993)
Spread of invading organisms: Patterns of spread. In: K.C.
Kim, ed., Evolution of Insect Pests, John Wiley & Sons Inc.,New York, PP.219-242.
Asayama, T., H. Tzuki, K. Ohishi and M. Takimoto (1984)
Population dynamics of rice water weevil. Research Bulletinof Aichi Agricultural Research Center (Special Issue).
15:18-24. (in Japanese)
Azuma, Y., K. Kimura and K. Tukamoto (1991) The action ofplant protection. In: Byogaityu hassei yosatu jigyo 50 syunen/ syokubutu boueki jigyo 40 syunen kinenkai, ed., The
History of Plant Protection in Japan, Byougaityu hassei
yosatu jigyo 50 syunen / syokubutu boueki jigyu 40 syunen
kinenkai, Tokyo, pp.118-126. (in Japanese)
Bowling, C.C. (1967) Insect pests of rice in the United States.
In: IRRI, ed., The major insect pests of the rice plant.
Proceedings of a Symposium at the IRRI, Sept. 1964, Johns
Hopkins Press, Baltimore, pp.551-570.
Carlton, J. T. (1996) Biological invasions and cryptogenic
species. Ecology. 77:1653-1655.
Ehrlich, P.R. (1988) Attributes of invaders and invading
processes. In: J. Drake, F. diCastri, R. Groves, F. Kruger, H.
Mooney, A. Rejmanek and M. Williamson, eds., BiologicalInvasions: A Global Perspective. John Wiley, Chichester,
pp.315-328.
Fenner, F. and F. N. Ratcliffe (1965) Myxomatosis. Cambridge
University Press, Cambridge.
Fukuyama, K. (1992) Insects in urban forests. Forest Science.

86

K. KIRITANI and N. MORIMOTO

4:33-36. (in Japanese)
Fukuyama, K. (1996) Relationship between urbanization anddefoliation by the fall webworm, Hyphantria cunea Drury(Lepidoptera:Arctiidae) on roadside trees. Applied
Entomology and Zoology. 40:83-84.
Gomi, T. (1996) The fall webworm. In: Zenkoku-NosonKyoiku-Kyokai, ed., Current topics on newly occurred
Takeda Chemical Industries, Ltd., agricultural pests in Japan,
Takeda Plant Protection Ser. 9, Tokyo, Japan. pp.108-184.
(in Japanese)Gomi, T. (1999) Seasonal adaptation and expansion of
distribution in the fall webworm, Hyphantria cunea in Japan.
In: E. Yano, K. Matsuo, M. Shiomi and D.A. Andow, eds.,
Biological invasions of ecosystem by pests and beneficialorganisms, National Institute of Agro-Environmental
Sciences Tsukuba, pp. 88-97.
Gomi, T. and M. Takeda (1996) Changes in life-history traits inthe fall webworm within half a century of introduction to
Japan. Functional Ecology. 10:384-389.
Harmey, J. H. and M. A. Harmey (1993) Detection andidentification of Bursaphelenchus species with DNA
fingerprinting and polymerase chain reaction. Journal of
Nematology. 25:406-415.
Hengeveld, B. (1989) Dynamics of biological invasions.
Chapman and Hall Ltd., New York.
Higo, S., A. Tanaka, S. Fukamachi and M. Horimoto (1986)
Ecology and methods of control of the rice water weevil,
Lissorhoptrus oryzophilus Kuschel in Kagoshima Prefecture.
1. Expansion of distribution range in 1985. Proceedings of
the Association for Plant Protection of Kyushu. 32:110-112.
(in Japanese)
Hirai, K. (1996) New pests of rice plants. In:
Zenkoku-Noson-Kyoiku-Kyokai, ed., Current topics on
newly occurred agricultural pests in Japan. Takeda Plant
Protection, Ser. 9, Takeda Chemical Industries, Ltd., Tokyo,
pp.33-42. (in Japanese)
Hirai, K. (2000) Rice water weevil. Nougyou oyobi Engei,
75:221-226. (in Japanese)
IPCC (2001) Climate change 2001, Cambridge Univ. Press.
Itô, Y. and I. Hattori (1973) Status of black-headed andred-headed types of Hyphantria cunea (Drury)(Lepidoptera:Arctiidae). III Distribution of various types andthe discussion on the relationship among them. Applied
Entomology and Zoology. 10:189-202.
Itô, Y. and K. Kiritani (1971) What does determine the numberof animals. NHK Publishing Co., Tokyo. (in Japanese)Itô, Y. and K. Miyashita (1968) Biology of Hyphantria cunea
Drury (Lepidoptera : Arctiidae) in Japan. V. Preliminary life
tables and mortality data in urban areas. Researches on
Population Ecology. 10:177-209.
Itoh, K. and T. Ohno (2003) Occurrence and pesticide
sensitivity of Echinothrips americanus on Perilla. Plant
Protection. 57:223-225.
Izawa, T., H. Kojima and M. Fukunaga (1984) Cultural control
methods of rice water weevil. Research Bulletin of Aichi
Agricultural Research Center (Special Issue). 15:82-86. (inJapanese)
Kaneko, K., K. Ishiguro, E. Taniguchi and H. Fuse (1984)
Invasion of the rice water weevil, Lissorhoptrus oryzophilus
Kuschel, in Shonai District in Yamagata Prefecture. Annual
Report of the Society of Plant Protection of North Japan.
35:94-96. (in Japanese)
Kayumi, J., K. Kiritani, T. Shimohata, H. Yasuda, H. Tsuzuki
and T. Asayama (1984) Studies on the population dynamics
of the rice water weevil, Lissorhoptrus oryzophilus Kuschell.
Japanese Journal of Applied Entomology and Zoology.
28:274-281. (in Japanese with English summary)
Kiritani, K. (1983) Colonizing insects: What makes a
successful colonizer? Insectarium. 20:310-317. (in Japanese)

Kiritani, K. (1998) Exotic Insects in Japan. Entomological
Science. 1:291-298.
Kiritani, K. (1999) Formation of exotic insect fauna in Japan.
In: E. Yano, K. Matsuo, M. Shiomi and D.A. Andow, eds.,
Biological invasions of ecosystem by pests and beneficialorganisms. National Institute of Agro-Environmental
Sciences, Tsukuba, pp.49-65.
Kiritani, K. (2000) Insect invasions in the world. Insectarium.
37:224-235. (in Japanese).
Kiritani, K. (2001) Invasive insect pests and plant quarantine inJapan. Extension Bulletin. Food and Fertilizer Technology
Center. 498:1-12.
Kiritani, K. (2002) List of alien species in Japan. In: The
Ecological Society of Japan, ed., Handbook of alien species
in Japan. Chijin-syokan, Tokyo, pp.306-312. (in Japanese)
Kiritani, K. and N. Morimoto (1993) Exotic insects in Japan.
Insectarium. 30:120-129. (in Japanese)
Kiritani, K. and K. Yamamura (2003) Exotic insects and theirpathways for invasion. In: G. Ruiz and J. Carlton, eds.,
Invasive Species: Vectors and Management Strategies. Island
Press, New York.
Kiritani, K. (in press) Invasive alien species issues. In:
Proceedings of International Symposium on “Forest insect
population dynamics and host influences” Joint Meeting of
IUFRO working groups. Sept 15-19, 2003, Kanazawa.
Kishi, Y. (1988) Pine wood nematode disease : A Monographon Matukui-mushi. Thomas Company, Tokyo. (in Japanese)
Kishimoto, R. (1980) Expansion of rice water weevil. Kongetu
no Noyaku. 24(12):50-54. (in Japanese)
Kiyohara, T. (1997) Pathogenicity and life cycle of
Bursaphelenchus xylophilus. In: H. Tamura, ed., Matsukuimushi (Pine wood nematode disease)–History and theachievement of recent researches. Association of Forest Pests
Control, Tokyo, pp.26-43. (in Japanese)
Kiyohara, T. and R.I. Bolla (1990) Pathogenic variability
among populations of the pinewood nematode,
Bursaphelenchus xylophilus. Forest Science. 36:1061-1076.
Kobayashi, F. (1978) Pine bark beetle problem in Japan,
referring to the discovery of the pine wood nematode,
Bursaphelenchus lignicolus (Mamiya & Kiyohara). Anzeiger
fuer Schadlingskunde Pflanzenschutz und Umweltschutz.
51:76-79.
Kobayashi, F. (1988) The Japanese pine sawyer. In: A.A.
Berryman, ed., Dynamics of forest insect populations.
Plenum Publishing Corporation, New York, pp.432-454.
Kobayashi, F., A. Yamane and T. Ikeda (1984) The Japanesepine sawyer beetle as the vector of pine wilt disease. Annual
Review of Entomology. 29:115-135.
Kobayashi, M. and T. Suzuki (1983) Seasonal prevalence ofrice water weevil (Lissorhoptrus oryzophilus Kuschel) in
Iwate Prefecture in 1982 and its possible course of invasion.
Annual Report of the Society of Plant Protection of North
Japan. 34:20-22. (in Japanese)
Kobayashi, S., G. Toyoshima and N. Morimoto (1997)
Occurrence and population density of the rice water weevil,
Lissorhoptrus
oryzophilus
Kuschel(Coleoptera:
Curculionidae) in the higher and lower elevation areas ofNagano Prefecture. Applied Entomology and Zoology.
32:9-18.
Konno, Y. (1998) Comparison of insecticide susceptibility
between fall webworm, Hyphantria cunea (Lepidoptera:
Arctiidae) and its parasitoid fly, Exorista japonica (Diptera:
Tachinidae). Japanese Journal of Applied Entomology andZoology. 42:167-170. (in Japanese with English summary)
Kunimi, Y. (1983) Spiders inhabiting the colonial-webs of thefall webworm, Hyphantria cunea Drury (Lepidoptera:
Arctiidae). Applied Entomology and Zoology. 18:81-89.
Lee, C.Y. and T.H. Chang (1989) Observation on the rice water
weevil, Lissorhoptrus oryzophilus Kuschel of Korea

Invasive Insect and Nematode Pests from North America(Coleoptera;
Curuculionidae).
KoreanJournalofEntomology. 16:15-18.
Lenski, R.E. and R.M. May (1994) The evolution of virulencein parasites and pathogens: Reconciliation between twocompeting hypotheses. Journal of theoretical Biology.
169:253-265.
MAFF (1996) Annual Report of forecasting of pest occurrences.
Ministry of Agriculture, Forestry and Fisheries, Tokyo. (inJapanese)
Makihara, H. (1997) Species and their bionomics of the vectorsof the pine wilt disease. In: H. Tamura, ed., Matsukui-mushi(Pine wood nematode disease)- History and the achievementof recent researches. Association of Forest Pests Control,
Tokyo, pp.44-64. (in Japanese)
Mamiya, Y. (1983) Pathology of the pine wilt disease caused by
Bursaphelenchus xylophilus (Nematoda: Aphelenchoididae).
Annual Review of Phytopathology. 21:201-220.
Masaki, S. (1975) Biology of Hyphantria cunea Drury(Lepidoptera: Arctiidae) in Japan: A review. Review of Plant
Protection Research. 8:14-28.
Masaki, S. (1977) Past and future. In: T. Hidaka, ed.,Adaptation and speciation of the fall webworm. Kodansha,
Tokyo. (in Japanese)
Matsui, M. (1985) Temperature dependence of flight muscle
development and flight activity of overwintered adults of therice water weevil, Lissorhoptrus oryzophilus Kuschel(Coleoptera: Curculionidae). Japanese Journal of Applied
Entomology and Zoology. 29:67-72. (in Japanese withEnglish summary)Mori, H. (1976) Establishment of Incisitermes minor in Tokyo.
Shiroari. 27:45-47. (in Japanese).
Morimoto, N. and K. Kiritani (1995) Fauna of exotic insects inJapan. Bulletin of National Institute of Agro-Environmental
Sciences. 12:87-120.
Morimoto, N., O. Imura and T. Kiura (1998) Potential effects
on global warming on the occurrence of Japanese pest insects.
Applied Entomology and Zoology. 33:147-155.
Morris, R.F. (1972) Predation by insects and spiders inhabitingcolonial webs of Hyphantria cunea. Canadian Entomologist.
104:1197-1207.
Muramatu, T. and M. Tao (1981) A long-distance flight of therice water weevil, Lissorhoptrus oryzophilus Kuschel.
Research Bulletin of the Plant Protection Service Japan.
17:57-62. (in Japanese with English summary)Naba, K., T. Yamaguchi, K. Hosotani, K. Nakazawa and K.
Umeda (1989) Ecology and control of the rice water weevil,
Lissorhoptrus oryzophilus Kuschel, in Hiroshima Prefecture,
2, Emigration of post-hibernating adults into paddy fields
and their egg deposition. Bulletin of the Hiroshima
Prefectural Agricultural Experiment Station. 52:19-26. (inJapanese with English summary)Nagai, K. and S. Teramoto (1985) Studies on the biology andmethods of control of the rice water weevil, Lissorhoptrus
oryzophilus Kuschel, in the warm region of Japan, 1,
Invasion and seasonal prevalence in Miyazaki Prefecture in
1984. Proceedings of the Association for Plant Protection of
Kyushu. 31:110-114. (in Japanese)
Ogawa, Y., K. Yokomizo and I. Ichikawa (1989) Seasonal
prevalence and control threshold of rice water weevil(Lissorhoptrus oryzophilus Kuschel) at different planting
dates in Nagasaki prefecture. Proceedings of the Association
for Plant Protection of Kyushu. 35:83-87. (in Japanese)
Ohbayashi, T. (2002) Alien insects in the Ogasawara islands.
In: The Ecological Society of Japan, ed., Handbook of alien
species in Japan, Chijin-syokan, Tokyo. pp.239-240.
Ohmura, W. and M. Tokoro (2003) Termite species invaded
Japan, Forest Science, 38:7-9.
Okada, T. (1980) Researches on the host plants of the ricewater weevil, Lissorhoptrus oryzophilus Kuschel, and on the87

behavior of the adult in the field. Bulletin of the Chugoku
National Agricultural Experiment Station Series E
Environment Division. 16:33-50. (in Japanese with English
summary)
Oliver, A.D. (1964) A behavioral study of two races of the fall
webworm, Hyphantria cunea (Lepidoptera : Arctiidae) in
Louisiana. Annals Entomological Society of America.
57:192-194.
Otake, A. (1999) Analytical study of fundatrix populations ofUroleucon
nigrotuberculatum(Olive)(Hemiptera:
Aphididae: Aphidinae) on an observation plot of thegoldenrod Solidago altissima L.. Applied Entomology andZoology. 34:435-442.
Ozaki, K. and T. Ohbayashi (2001) DNA comparison ofJapanese populations of Hyphantria cunea with divergent
life cycles. Entomological Science. 4:47-52.
Shaku, I., T. Koumura, M. Takamura, T. Asayama, H. Tsuzuki
and K. Ohishi (1984 )Screening of the resistant varieties tothe rice water weevil. Research Bulletin of Aichi Agricultural
Research Center. 15:96-99. (in Japanese)
Shigesada, N. (1992) Mathematical modeling for biologicalinvasions. University of Tokyo Press, Tokyo. (In Japanese)
Shimohata, T. and M. Hanoh (1983) Effects of surfece drainage
on suppression of the density of the rice water weevil.
Proceedings of the Kansai Plant Protection Society. 25:18.
(in Japanese)
Shih, H.P. (1991) The newly found rice water weevil(Lissorhoptrus oryzophilus Kuschel) on rice plant in Taiwan.
Bulletin of Taiwan Agricultural Improvement Station.
7:61-67.
Sugimoto, S. (1995) Aphids (Homoptera: Aphididae) collectedin the Ryukyu Islands, Japan with their host plants andlocalities. Rostria. 44: 5-18. (in Japanese)
Sugimoto, S. (1999) Occurrence of Illinoia liriodendri (Monell)(Homoptera: Aphididae) in Japan. Entomological Science.
2:89-91.
Sun, Y-C. (1982) Occurrence of the pine wood nematode in
Chung Shan mausoleum in Nanjin. Jiangsu Forest Science.
7:47.
Tate, K. (2001) Occurrence of the fall webworm in Hakodate,
Hokkaido. Forest pest. 50:71-72.
Takara, T. (1954) The introduction and pest management ofOmphisa anastomosalis and Euscepes postfasciatus. Plant
Protection. 8:436-438. (in Japanese)
Takasu, F., N. Yamamoto, K. Kawasaki, K. Togashi, Y. Kishi
and N. Shigesada (2000) Modeling the expansion of an
introduced tree disease. Biological Invasions. 2:141-150.
Taketani, A., M. Okuda and R. Hosoda (1975) The
meteorological analysis on the epidemic mortality of pinetrees, with special reference to the effective accumulated
temperature. Journal of Japanese Forest Society. 57:169-176.
(in Japanese with English summary)Tarès, S., J. M. Lemontey, G. De. Guiran and P. Abad (1993)
Cloning and characterization of a highly conserved satellite
DNA sequence specific for the phytoparasitic nematode
Bursaphelenchus xylophilus. Gene. 129:269-273.
Toda, T. (1997) Breeding of resistant pine trees resistant to thepine wood nematode. In: T. Tamura, ed., Matsukui-mushi(Pine wood nematode disease)- History and the achievementof recent researches. Association of Forest Pests Control,
Tokyo, pp.168-272. (in Japanese)
Togashi, K. (1989) Studies on population dynamics of
Monochamus alternatus Hope (Coleoptera: Cerambycidae)
and spread of pine wilt disease caused by Bursaphelenchus
xylophilus (Nematoda: Aphelenchoididae). Bulletin of
Ishikawa-Ken Forest Experimental Station. 20:1-142. (inJapanese with English summary)Togashi, K. (2002) Life history of Japanese Pine Sawyer,
Monochamus alternatus, and characteristics of larval food88

K. KIRITANI and N. MORIMOTO

resources. Japanese Journal of Ecology. 52:69-74.
Tsuzuki, H., T. Amano, T. Asayama and Y. Isogawa (1984) A
record and expansion of distribution of rice water weevil.
Research Bulletin of Aichi Agricultural Research Center(Special Issue), 15:5-8. (in Japanese)
Uezumi, Y. (1976) The first outbreak of Hyphantria cunea
Drury in Nara Prefecture. Plant Protection. 31: 355-356. (inJapanese)van Lenteren, J.C. (1995) Frequency and consequences of
insect invasions. In: H.M.T. Hokkanen and J.M. Lynch, eds.,
Biological control: Benefits and Risks, Cambridge University
Press, Cambridge, pp.30-43.
Warren, L.O. and M. Tadic (1970) The fall webworm,
Hyphantria cunea (Drury). Arkansas Agricultural
Experiment Station Bulletin. 759:1-106.
Warren, L.O., W.B. Peck and M. Tadic (1967) Spiders
associated with the fall webworm, Hyphantria cunea(Lepidoptera: Arctiidae). Journal of Kansas EntomologicalSociety. 40:382-395.
Williamson, M. (1996) Biological invasions. Chapman andHall, London.
Wingfield, M.J., R.A. Blanchette, T.H. Nicholls and K. Robbins(1982) The pine wood nematode: A comparison of thesituation in the United States and Japan. Canadian Journal ofForest Research. 12: 71-75.
Yamamura, K. and K. Kiritani (1998) A simple method toestimate the potential increase in the number of generations
under global warming in temperate zones. Applied
Entomology and Zoology. 33:289-298.
Yamanaka, M., N. Fujiyoshi and K. Yoshida (1985) Invasion,
dissemination, increase of density and seasonal trend of
occurrence of the rice water weevil, Lissorhoptrus
oryzophilus Kuschel in Fukuoka Prefecture. Proceedings of
the Association for Plant Protection of Kyushu. 31:106-109.
(in Japanese)(Received 10 December 2003, Accepted 3 February 2004)